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Journal ArticleDOI

Intracortical and Thalamocortical Connections of the Hand and Face Representations in Somatosensory Area 3b of Macaque Monkeys and Effects of Chronic Spinal Cord Injuries.

30 Sep 2015-The Journal of Neuroscience (Society for Neuroscience)-Vol. 35, Iss: 39, pp 13475-13486
TL;DR: It is shown that reorganization of primary somatosensory area 3b is not accompanied with either an increase in intrinsic cortical connections between the hand and face representations, or any change in thalamocortical inputs to these areas.
Abstract: Brains of adult monkeys with chronic lesions of dorsal columns of spinal cord at cervical levels undergo large-scale reorganization. Reorganization results in expansion of intact chin inputs, which reactivate neurons in the deafferented hand representation in the primary somatosensory cortex (area 3b), ventroposterior nucleus of the thalamus and cuneate nucleus of the brainstem. A likely contributing mechanism for this large-scale plasticity is sprouting of axons across the hand-face border. Here we determined whether such sprouting takes place in area 3b. We first determined the extent of intrinsic corticocortical connectivity between the hand and the face representations in normal area 3b. Small amounts of neuroanatomical tracers were injected in these representations close to the electrophysiologically determined hand-face border. Locations of the labeled neurons were mapped with respect to the detailed electrophysiological somatotopic maps and histologically determined hand-face border revealed in sections of the flattened cortex stained for myelin. Results show that intracortical projections across the hand-face border are few. In monkeys with chronic unilateral lesions of the dorsal columns and expanded chin representation, connections across the hand-face border were not different compared with normal monkeys. Thalamocortical connections from the hand and face representations in the ventroposterior nucleus to area 3b also remained unaltered after injury. The results show that sprouting of intrinsic connections in area 3b or the thalamocortical inputs does not contribute to large-scale cortical plasticity. Significance statement: Long-term injuries to dorsal spinal cord in adult primates result in large-scale somatotopic reorganization due to which chin inputs expand into the deafferented hand region. Reorganization takes place in multiple cortical areas, and thalamic and medullary nuclei. To what extent this brain reorganization due to dorsal column injuries is related to axonal sprouting is not known. Here we show that reorganization of primary somatosensory area 3b is not accompanied with either an increase in intrinsic cortical connections between the hand and face representations, or any change in thalamocortical inputs to these areas. Axonal sprouting that causes reorganization likely takes place at subthalamic levels.
Citations
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Journal ArticleDOI
TL;DR: It is concluded that the cortical representation of the limb remains remarkably stable despite the loss of its main peripheral input and the implications of the stability of sensory representations on the development of upper-limb neuroprostheses.

109 citations


Cites background from "Intracortical and Thalamocortical C..."

  • ...In fact, there is little anatomical evidence that the face-elicited activity in SI is mediated by the growth of new cortico-cortical projections: Very few axons cross the face–hand boundary in SI of intact animals (see [57] for analogous results in humans revealed with neuroimaging) and deafferentation of the hand region does not result in any measurable increase in these boundary-crossing projections [58]....

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Journal ArticleDOI
23 Aug 2016-eLife
TL;DR: It is shown that representation of the missing hand’s individual fingers persists in the primary somatosensory cortex even decades after arm amputation, questions the extent to which continued sensory input is necessary to maintain organisation in sensory cortex, thereby reopening the question what happens to a cortical territory once its main input is lost.
Abstract: The hand area of the primary somatosensory cortex contains detailed finger topography, thought to be shaped and maintained by daily life experience. Here we utilise phantom sensations and ultra high-field neuroimaging to uncover preserved, though latent, representation of amputees' missing hand. We show that representation of the missing hand's individual fingers persists in the primary somatosensory cortex even decades after arm amputation. By demonstrating stable topography despite amputation, our finding questions the extent to which continued sensory input is necessary to maintain organisation in sensory cortex, thereby reopening the question what happens to a cortical territory once its main input is lost. The discovery of persistent digit topography of amputees' missing hand could be exploited for the development of intuitive and fine-grained control of neuroprosthetics, requiring neural signals of individual digits.

97 citations


Cites background from "Intracortical and Thalamocortical C..."

  • ...…more limited than initially thought, and that instead the functional changes previously observed in S1 following input loss could be attributed to reorganisation in sub-cortical areas in the afferent pathway, principally the brainstem (Jain et al., 1998; Kambi et al., 2014; Chand and Jain, 2015)....

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Journal ArticleDOI
TL;DR: The need to consider potential contributions of additional brain mechanisms, beyond S1 remapping, and the dynamic interplay of contextual factors with brain changes for understanding and alleviating PLP is highlighted.

70 citations


Cites background from "Intracortical and Thalamocortical C..."

  • ...It has been suggested that the initial remapping triggered by deprivation will become refined by inputs due to daily hand usage involving compensatory behaviours (Churchill et al., 1998; Elbert et al., 1997)....

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Journal ArticleDOI
TL;DR: The data extend the Brodmann model in human sensorimotor cortex and suggest that body parts are an important organizing principle, similar to the distinction between sensory and motor processing.
Abstract: The cytoarchitectonic map as proposed by Brodmann currently dominates models of human sensorimotor cortical structure, function, and plasticity. According to this model, primary motor cortex, area 4, and primary somatosensory cortex, area 3b, are homogenous areas, with the major division lying between the two. Accumulating empirical and theoretical evidence, however, has begun to question the validity of the Brodmann map for various cortical areas. Here, we combined in vivo cortical myelin mapping with functional connectivity analyses and topographic mapping techniques to reassess the validity of the Brodmann map in human primary sensorimotor cortex. We provide empirical evidence that area 4 and area 3b are not homogenous, but are subdivided into distinct cortical fields, each representing a major body part (the hand and the face). Myelin reductions at the hand-face borders are cortical layer-specific, and coincide with intrinsic functional connectivity borders as defined using large-scale resting state analyses. Our data extend the Brodmann model in human sensorimotor cortex and suggest that body parts are an important organizing principle, similar to the distinction between sensory and motor processing.

63 citations


Cites background from "Intracortical and Thalamocortical C..."

  • ...However, a recent definitive study showed that in monkeys with chronic lesions of the dorsal column of spinal cord that had resulted in large-scale map reorganization of hand and face representations in area 3b, nevertheless showed a striking absence of new intracortical projections across the hand–face border (Chand and Jain 2015)....

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Journal ArticleDOI
TL;DR: This review focuses on the reorganization of cortical networks observed after injury and posits a role of intracortical circuits in recovery.

31 citations

References
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Journal ArticleDOI
TL;DR: This study examined cortical connections of areas 3b and 1 in 17 macaque monkeys in reference to regional somatotopography by injecting fluorescent retrograde tracers and anterograde tracer Rhodamine Dextran into cutaneously responsive sites in primary somatosensory cortex.
Abstract: This study examined cortical connections of areas 3b and 1 in 17 macaque monkeys in reference to regional somatotopography. The fluorescent retrograde tracers Fast Blue and Diamidino Yellow and the anterograde tracer Rhodamine Dextran were injected into closely related cutaneously responsive sites in primary somatosensory cortex, e. g., adjacent digits. Supra- and infragranular layers in nearly all studied areas contained labeled pyramidal cells. Labeled infragranular cells predominated at the fringes of a distribution where cells labeled from different tracer injections in the same brain intermixed more. All topographical regions across area 1 have reciprocal connections with areas 4, 3a, 3b, 1, 2, and 5. Intrinsic connections within area 1 and between it and area 2 are greatest; those with area 3b are less. Intrinsic connections within area 3b exceed all other nearby projections from this area which reciprocally connects with areas 3a, 1 and 2. Connections appear topographically organized, including those with poorly mapped regions, like area 5. These connections link representations of neighboring skin and skip map regions that include disjoint dermatomal areas. Connections from adjacent digit representations overlap; however, double-labeled cells were not found. Distal and proximal digit zones mostly interconnect within an area. Intrinsic connections spread further in area 1 than in area 3b, thereby joining more disparate topographical zones than interareal connections, which project more homotopically. The domain over which the map in somatosensory cortical area I (SI) dynamically changes following in tracortical microstimulation (Recanzone, Merzenich and Dinse, Cerebral Cortex 2:181-196, 1992) may depend on the range of intrinsic connections observed in this study. The extent of connections between cortical areas was less than expected and this challenges the hypothesis that these connections directly create receptive field enlargements.

144 citations


"Intracortical and Thalamocortical C..." refers background in this paper

  • ...Role of intrinsic connections in plasticity Intrinsic connections likely contribute to the brain reorganization (Burton and Fabri, 1995; Jones and Pons, 1998)....

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  • ...These locations correspond to representations of D1 and chin in the VP nucleus (Jones and Friedman, 1982; Kaas et al., 1984; Darian-Smith et al., 1990; Burton and Fabri, 1995; Padberg et al., 2009)....

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  • ...In studies where intrinsic connections of the hand representation in area 3b were determined without explicit goal of determining connections across the hand–face border (Burton and Fabri, 1995; Liao et al., 2013; Négyessy et al., 2013), the lateral extent of labeled neurons shows a sharp boundary corresponding to the expected location of the hand–face border....

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  • ...…connections of the hand representation in area 3b were determined without explicit goal of determining connections across the hand–face border (Burton and Fabri, 1995; Liao et al., 2013; Négyessy et al., 2013), the lateral extent of labeled neurons shows a sharp boundary corresponding to…...

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Journal ArticleDOI
TL;DR: Anterograde and retrograde tracing with biotinylated dextran amine and Phaseolus vulgaris leukoagglutinin was used to assess projection patterns within the vibrissae representation of the rat's primary somatosensorycortex, and there was a tendency for labelling to be more extensive along the represented of the row of vibrISSae follicles that included the injection site than across rows.
Abstract: Anterograde and retrograde tracing with biotinylated dextran amine and Phaseolus vulgaris leukoagglutinin was used to assess projection patterns within the vibrissae representation of the rat's primary somatosensory cortex (S-I). Large and small injections of either tracer into the center of the vibrissae representation yielded dense anterograde and retrograde labelling throughout much of the tangential extent of the vibrissae representation within S-I. In all layers, the pattern and extent of retrograde and anterograde label was in rough congruence. The organization of this labelling varied across cortical layers. In layers II and III, labelled fibers extended away from injection sites in all directions and yielded a uniform pattern, which decreased in density with increasing distance from the tracer injection. There was a tendency for labelling to be more extensive along the representation of the row of vibrissae follicles that included the injection site than across rows. There was also a tendency for anterograde labelling to be more extensive in the direction of the representation of follicles more rostral on the face than that injected. In lamina IV, both labelled fibers and cells were restricted for the most part to the septa regions between the barrels. However, a small number of retrogradely labelled neurons were also located in the barrels (approximately one-ninth of the number found in the septa). The pattern observed in laminae II-III was repeated in layers V and VI. In these laminae, there was no evidence of a pattern of intracortical connections related to the vibrissae representation in overlying lamina IV.

115 citations


"Intracortical and Thalamocortical C..." refers background in this paper

  • ...In rat whisker barrel cortex, whisker pairing plasticity is more robust across rows compared with across arcs (Armstrong-James et al., 1994), which corresponds with richer intrinsic connections across rows than arcs (Hoeflinger et al., 1995)....

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Journal ArticleDOI
TL;DR: Thalamic connections of three subdivisions of somatosensory cortex in marmosets were determined by placing wheatgerm agglutinin conjugated with horseradish peroxidase and fluorescent dyes as tracers into electrophysiologically identified sites in S‐I, S‐II, and the parietal ventral area, PV.
Abstract: Thalamic connections of three subdivisions of somatosensory cortex in marmosets were determined by placing wheatgerm agglutinin conjugated with horseradish peroxidase and fluorescent dyes as tracers into electrophysiologically identified sites in S-I (area 3b), S-II, and the parietal ventral area, PV. The relation of the resulting patterns of transported label to the cytoarchitecture and cytochrome oxidase architecture of the thalamus lead to three major conclusions. 1) The region traditionally described as the ventroposterior nucleus (VP) is a composite of VP proper and parts of the ventroposterior inferior nucleus (VPi). Much of the VP region consists of groups of densely stained, closely packed neurons that project to S-I. VPi includes a ventral oval of pale, less densely packed neurons and finger-like protrusions that extend into VP proper and separate clusters of VP neurons related to different body parts. Neurons in both parts of VPi project to S-II rather than S-I. Connection patterns indicate that the proper and the embedded parts of VPi combine to form a body representation paralleling that in VP. 2) VPi also provides the major thalamic input into PV. 3) In architecture, location, and cortical connections, the region traditionally described as the anterior pulvinar (AP) of monkeys resembles the medial posterior nucleus, Pom, of other mammals and we propose that all or most of AP is homologous to Pom. AP caps VP dorsomedially, has neurons that are moderately dense in Nissl staining, and reacts moderately in CO preparations. AP neurons project to S-I, S-II, and PV in somatotopic patterns.

112 citations


"Intracortical and Thalamocortical C..." refers result in this paper

  • ...Normal thalamocortical connections and the somatotopy in the VP nucleus of thalamus have been described by many laboratories, and our data conform to previous reports (Jones and Friedman, 1982; Darian-Smith et al., 1990; Krubitzer and Kaas, 1992; Padberg et al., 2009; Cerkevich et al., 2013)....

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Journal ArticleDOI
01 Apr 1999-Neuron
TL;DR: Evidence from noninvasive is capable of extensive reorganization came from a reimaging of evoked activity in the brains of humans with port of a single raccoon that had lost a forearm at some arm amputations that cortex formerly devoted to the unknown time prior to its capture.

110 citations


"Intracortical and Thalamocortical C..." refers background in this paper

  • ...Axonal sprouting that causes reorganization likely takes place at subthalamic levels. the thalamus (Jones and Pons, 1998; Kaas et al., 1999; Jain et al., 2008), and cuneate nucleus of the brainstem (Kambi et al., 2014)....

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  • ...…such as transection of the dorsal columns (10 –14 mm, and sometimes more that 20 mm, Jain et al., 2008) or transection of dorsal roots (Pons et al., 1991), is beyond what can be mediated by normal connections in the brain, reorganization must involve axonal sprouting (Kaas et al., 1999)....

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  • ...…at multiple sites along the somatosensory pathway, it has been proposed that reorganization could take place at all these sites independently, or changes at upstream areas could be a reflection of the downstream reorganization (Pons et al., 1991; Kaas et al., 1999; Jones, 2000; Kambi et al., 2014)....

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Journal ArticleDOI
TL;DR: It is concluded that the anatomical isomorph for the body surface representation in area 3B is a reliable reflection of normal cortical organization and may be a common feature of the primate area 3b.
Abstract: An isomorph of the glabrous hand is visible in primary somatosensory cortex (area 3b) of owl monkeys in brain sections cut parallel to the surface and stained for myelin. A mediolateral row of five ovals, separated by myelin-light septa, represents digits and corresponds precisely with cortical sites activated by light touch on individual digits in microelectrode recordings. A number of caudal ovals relate to pads of the palm. A more distinct septum separates the hand from the more lateral face representation. Within the face representation, two large myelin-dense ovals can be identified that are activated by the upper or lower face in a caudo-rostral sequence. Accidental finger loss or dorsal column section, deafferentations that result in reorganization of the physiological map in area 3b, do not alter the morphological map. The proportions for each digit and palm in the morphological map do not vary across normal and deafferented animals. Similar isomorphs were also seen in area 3b of squirrel and macaque monkeys. We conclude that the anatomical isomorph for the body surface representation in area 3b is a reliable reflection of normal cortical organization and may be a common feature of the primate area 3b. The isomorph can provide a reference in studies of somatotopic reorganization.

104 citations